Search

Plant root nodule symbiosis (RNS) with mutualistic nitrogen-fixing bacteria is restricted to a single clade of angiosperms, the Nitrogen-Fixing Nodulation Clade (NFNC), and is best understood in the legume family. It is widely accepted that nodulation originated through the assembly of modules recruited from existing functions, such as mycorrhizal symbiosis, polar growth, and lateral root development. Because nodulating species are scattered within the NFNC, the number of times nodulation has evolved or has been lost has been a matter of considerable speculation. This interesting evolutionary question has practical implications concerning the ease with which nodulation might be engineered in non-nodulating crop plants. Nodulating species share many commonalities, due either to divergence from a common ancestor over 100 million years ago or to convergence or deep homology following independent origins over that same time period. In either case, comparative analyses of diverse nodulation syndromes can provide insights into constraints on nodulation—what must be acquired or cannot be lost for a functional symbiosis—and what the latitude is for variation in the symbiosis. However, much remains to be learned about nodulation, especially outside of legumes. Here we present new information across the spectrum of nodulating groups. We find no evidence for convergence at the level of amino acid residues or gene family expansion across the NFNC. Our phylogenomic analyses further emphasize the uniqueness of the transcription factor, NIN, as a master regulator of nodulation, and identify key mutations affecting its function across the NFNC. We find that nodulation genes are over-represented among orthologous gene groups (OGs) present in the NFNC common ancestor, but that lineage-specific OGs play major roles in nodulation. We identified over 900,000 conserved noncoding elements (CNEs), of which over 300,000 were unique to NFNC species. A significant proportion of these are associated with nodulation-related genes and thus are candidates for transcriptional regulators.

The filamentous and unicellular algae of the class Zygnematophyceae are the closest algal relatives of land plants. Inferring the properties of the last common ancestor shared by these algae and land plants allows us to identify decisive traits that enabled the conquest of land by plants. We sequenced four genomes of filamentous Zygnematophyceae (three strains ofZygnema circumcarinatumand one strain ofZ. cylindricum) and generated chromosome-scale assemblies for all strains of the emerging model systemZ. circumcarinatum. Comparative genomic analyses reveal expanded genes for signaling cascades, environmental response, and intracellular trafficking that we associate with multicellularity. Gene family analyses suggest that Zygnematophyceae share all the major enzymes with land plants for cell wall polysaccharide synthesis, degradation, and modifications; most of the enzymes for cell wall innovations, especially for polysaccharide backbone synthesis, were gained more than 700 million years ago. In Zygnematophyceae, these enzyme families expanded, forming co-expressed modules. Transcriptomic profiling of over 19 growth conditions combined with co-expression network analyses uncover cohorts of genes that unite environmental signaling with multicellular developmental programs. Our data shed light on a molecular chassis that balances environmental response and growth modulation across more than 600 million years of streptophyte evolution.HIGHLIGHTSGenomes of four filamentous algae (Zygnema) sisters to land plantsZygnemaare rich in genes for multicellular growth and environmental acclimation: signaling, lipid modification, and transportCell wall innovations: diversification of hexameric rosette cellulose synthase in ZygnematophyceaeCo-expression networks reveal conserved modules for balancing growth and acclimation

SummarySymbiotic interactions have structured past and present ecosystems and shaped the evolution of life. As any trait, the symbiotic state observed in extant species builds on ancestral and conserved features, and lineage-specific innovations. From these mixed origins, defining the ancestral state of symbiotic associations is challenging although it is instrumental for understanding how symbiotic abilities emerge from non-symbiotic states. Here we aimed at reconstructing the intermediate steps leading to the root-nodule nitrogen-fixing symbiosis (RNS) observed in some extant flowering plants. For this, we compared the transcriptomic responses of nine host plants in response to symbiotic bacteria. We included the mimosoid legume Mimosa pudica for which we assembled a chromosome-level genome and generated the transcriptomic response to experimentally evolved bacterial symbionts. With this dataset, we reconstructed the ancestral RNS transcriptome, composed of most already described symbiotic genes together with hundreds of novel candidates. We found that the response to the chemical signals produced by the symbiont, nodule organogenesis and nitrogen-fixation are predominantly linked to ancestral responses, although these traits have diversified in the different nitrogen-fixing lineages. We detected a clear signature of recent and convergent evolution for the ability to release intracellular symbiosomes in two legume lineages, exemplified by the expression of different classes of small proteins in each group, potentially leading to the convergent gain of symbiotic evolutionary stability. Our findings demonstrate that most of the novelties for RNS were mostly in place in the most recent common ancestor of the RNS-forming species that lived on Earth 110 million years ago.Graphical abstractA little graphical/nice phylogeny with nodes of interestHighlightsWe sequenced a high-quality genome of the Mimosoideae Mimosa pudicaThe nitrogen-fixing root-nodule symbiosis relies on an ancestral transcriptomic responseAll symbiotic traits involve genes of the ancestral symbiotic programSymbiont perception, nodule organogenesis and nitrogen-fixation are essentially ancestral processesConvergent evolution of intracellular accommodation of symbionts additionally involves lineage-specific genes

Phosphate (Pi) deficiency is a major factor limiting plant productivity worldwide. Land plants have evolved different strategies to cope with Pi deficiency. For instance, plants activate the so-called Pi starvation response (PSR) system, which is regulated by the transcription factor Phosphate Starvation Response1 (PHR1), to adjust plant growth and metabolic activity accordingly. Additionally, land plants can also establish mutualistic associations with soil microbes able to solubilize Pi from plant-inaccessible soil complexes and to transfer it to the host plant. A growing body of evidence indicates that PHR1 and the PSR system not only regulate the plant responses to Pi deficiency in an abiotic context, but they are also crucial for plants to properly interact with beneficial soil microbes able to provide them with soluble Pi. Recent evidence indicates that PHR1 and the PSR system contribute to shaping the plant-associated microbiota through the modulation of the plant immune system. The PSR and immune system outputs are tightly integrated by PHR1. Here, we review how plant host Pi status influences the establishment of the mutualistic association with soil microbes. We also highlight the role of PHR1 and the PSR system in shaping both the root microbiome and plant responses to Pi deficiency.

The Zygnematophyceae is the sister clade to the land plants, but their biology remains mysterious. In a new study, a resolved phylogeny and a scenario for the evolution of multicellularity in that clade are proposed.

Plant hormone signaling pathways have diversified during plant evolution. A new study reveals conservation of DELLA functions in growth and environmental stress responses across land plants.

The root nodule symbiosis (RNS) of plants with nitrogen-fixing bacteria is phylogenetically restricted to a single clade of flowering plants, which calls for yet unidentified trait acquisitions and genetic changes in the last common ancestor. Here we discovered – within the promoter of the transcription factor gene Nodule Inception (NIN) – a cis-regulatory element (PACE), exclusively present in members of this clade. PACE was essential for restoring infection threads (ITs) in nin mutants of the legume Lotus japonicus. PACE sequence variants from RNS-competent species appeared functionally equivalent. Evolutionary loss or mutation of PACE is associated with loss of this symbiosis. During early stages of nodule development, PACE dictates gene expression in a spatially restricted domain containing cortical cells carrying ITs. Consistent with its expression domain, PACE-driven NIN expression restored the formation of cortical ITs, also when engineered into the NIN promoter of tomato. Our data pinpoint PACE as a key evolutionary invention that connected NIN to a pre-existing symbiosis signal transduction cascade that governs the intracellular accommodation of arbuscular mycorrhiza fungi and is conserved throughout land plants. This connection enabled bacterial uptake into plant cells via intracellular support structures like ITs, a unique and unifying feature of this symbiosis.

Organization of membrane topologies in plants has so far been mainly attributed to the cell wall and the cytoskeleton. Taking rhizobial infections of legume root cells, where plasma membranes undergo dynamic and large-scale topology changes, as an initial model, we challenged this paradigm and tested whether additional scaffolds such as plant-specific remorins that accumulate on highly curved and often wall-less plasma membrane domains, control local membrane dynamics. Indeed, loss-of-function mutants of the remorin protein SYMREM1 failed to develop stabilized membrane tubes as found in colonized cells in wild-type plants, but released empty membrane spheres instead. Expression of this and other remorins in wall-less protoplasts allowed engineering different membrane topologies ranging from membrane blebs to long membrane tubes. Reciprocally, mechanically induced membrane indentations were equally stabilized by SYMREM1. This function is likely supported by remorin oligomerization into antiparallel dimers and the formation of higher order membrane scaffolding structures. Taken together we describe an evolutionary confined mechanism that allows the stabilization of large-scale membrane conformations and curvatures in plants.One-sentence summaryThe remorin SYMREM1 evolved as structural membrane scaffold that stabilizes membrane tubulation and curvature during symbiotic intracellular infections.

SummaryMutualistic symbioses, such as lichens formed between fungi and green algae or cyanobacteria, have contributed to major transitions in the evolution of life and are at the center of extant ecosystems. However, our understanding of their evolution and function remains elusive in most cases. Here, we investigated the evolutionary history and the molecular innovations at the origin of lichens in green algae. We de novo sequenced the genomes or transcriptomes of 12 lichen-forming and closely related non-lichen-forming algae and performed comparative phylogenomics with 22 genomes previously generated. We identified 39 functional categories and 11 orthogroups significantly enriched in lichen-forming chlorophyte green algae. Among them, functions such as carbohydrates metabolism and stress tolerance could be related to the pioneer characteristics of lichens. We detected lichen-specific expansions of glycosyde hydrolase gene families known to remodel cell walls, including the glycosyde hydrolase 8 (GH8) which encodes a glucanase and was acquired in lichenizing Trebouxiophyceae by horizontal gene transfer from bacteria, concomitantly with the ability to form lichens. Mining genome-wide orthogroups, we found additional evidence supporting at least two independent origins of lichen-forming ability in chlorophyte green algae.HighlightsWe sequenced 12 lichen-forming and non-lichen-forming chlorophytesLichens evolved independently in Ulvophyceae and TrebouxiophyceaeGene family expansion correlate with the ability to form lichensHorizontal Gene Transfer of a glycoside hydrolase is linked with lichenization

Nitrogen is an essential macronutrient and a key cellular messenger. Plants have evolved refined molecular systems to sense the cellular nitrogen status. This is exemplified by the root nodule symbiosis between legumes and symbiotic rhizobia, where nitrate availability inhibits this mutualistic interaction. Additionally, nitrate also functions as a metabolic messenger, resulting in nitrate signaling cascades which intensively crosstalk with other physiological pathways. Nodule inception-like proteins (NLPs) are key players in nitrate signaling and regulate nitrate-dependent transcription during legume-rhizobia interactions. Nevertheless, the coordinated interplay between nitrate signaling pathways and rhizobacteria-induced responses remains to be elucidated. In our study, we investigated rhizobia-induced changes in the root system architecture of the non-legume host arabidopsis under different nitrate conditions. We demonstrate that rhizobium-induced lateral root growth and increased root hair length and density are regulated by a nitrate-related signaling pathway. Key players in this process are

Nitrogen is an essential macronutrient and a key cellular messenger. Plants have evolved refined molecular systems to sense the cellular nitrogen status. This is exemplified by the root nodule symbiosis between legumes and symbiotic rhizobia, where nitrate availability inhibits this mutualistic interaction. Additionally, nitrate also functions as a metabolic messenger, resulting in nitrate signaling cascades which intensively crosstalk with other physiological pathways. Nodule inception-like proteins (NLPs) are key players in nitrate signaling and regulate nitrate-dependent transcription during legume–rhizobia interactions. Nevertheless, the coordinated interplay between nitrate signaling pathways and rhizobacteria-induced responses remains to be elucidated. In our study, we investigated rhizobia-induced changes in the root system architecture of the non-legume host arabidopsis under different nitrate conditions. We demonstrate that rhizobium-induced lateral root growth and increased root hair length and density are regulated by a nitrate-related signaling pathway. Key players in this process are AtNLP4 and AtNLP5, because the corresponding mutants failed to respond to rhizobia. At the cellular level, AtNLP4 and AtNLP5 control a rhizobia-induced decrease in cell elongation rates, while additional cell divisions occurred independently of AtNLP4. In summary, our data suggest that root morphological responses to rhizobia are coordinated by a newly considered nitrate-related NLP pathway that is evolutionarily linked to regulatory circuits described in legumes. [Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY 4.0 International license .

In flowering plants, carotenoid-derived strigolactones (SLs) have dual functions as hormones that regulate growth and development, and as rhizosphere signaling molecules that induce symbiosis with arbuscular mycorrhizal (AM) fungi. Here, we report the identification of bryosymbiol (BSB), a previously unidentified SL from the bryophyte Marchantia paleacea. BSB is also found in vascular plants, indicating that it is ancestral in land plants. BSB synthesis is enhanced at AM symbiosis permissive conditions and BSB deficient mutants are impaired in AM symbiosis. In contrast, the absence of BSB synthesis has little effect on the growth and gene expression. We show that the introduction of the SL receptor of Arabidopsis renders M. paleacea cells BSB-responsive. These results suggest that BSB is not perceived by M. paleacea cells due to the lack of cognate SL receptors. We propose that SLs originated as AM symbiosis-inducing rhizosphere signaling molecules and were later recruited as plant hormone.

Summary Legumes have maintained the ability to associate with rhizobia to sustain the nitrogen-fixing root nodule symbiosis (RNS). In Medicago truncatula, the Nod factor (NF)-dependent intracellular root colonization by Sinorhizobium meliloti initiates from young, growing root hairs. They form rhizobial traps by physically curling around the symbiont.1,2 Although alterations in root hair morphology like branching and swelling have been observed in other plants in response to drug treatments3 or genetic perturbations,4, 5, 6 full root hair curling represents a rather specific invention in legumes. The entrapment of the symbiont completes with its full enclosure in a structure called the “infection chamber” (IC),1,2,7,8 from which a tube-like membrane channel, the “infection thread” (IT), initiates.1,2,9 All steps of rhizobium-induced root hair alterations are aided by a tip-localized cytosolic calcium gradient,10,11 global actin re-arrangements, and dense subapical fine actin bundles that are required for the delivery of Golgi-derived vesicles to the root hair tip.7,12, 13, 14 Altered actin dynamics during early responses to NFs or rhizobia have mostly been shown in mutants that are affected in the actin-related SCAR/WAVE complex.15, 16, 17, 18 Here, we identified a polarly localized SYMBIOTIC FORMIN 1 (SYFO1) to be required for NF-dependent alterations in membrane organization and symbiotic root hair responses. We demonstrate that SYFO1 mediates a continuum between the plasma membrane and the cell wall that is required for the onset of rhizobial infections., Graphical abstract, Highlights • The SYMBIOTIC FORMIN 1 (SYFO1) specifically regulates symbiotic root hair curling • SYFO1 directly binds actin and polarizes in responding root hairs • SYFO1 induces membrane protrusions in cell-wall-devoid protoplasts • Cell wall association of SYFO1 is indispensable for its function in root hairs, Here, Liang et al. report that the formin SYFO1 specifically regulates polar actin alignments during symbiotic root hair responses in Medicago truncatula. Although SYFO1 is able to induce membrane protrusions in protoplasts, its endogenous function requires an association with the cell wall.

New pathways in plants and microbes Plants and microbes have interacted through evolution in ways that shaped diversity and helped plants colonize land. Delaux and Schornack review how insights from a range of plant and algal genomes reveal sustained use through evolution of ancient gene modules as well as emergence of lineage-specific specializations. Mosses, liverworts, and hornworts have layered innovation onto existing pathways to build new microbial interactions. Such innovations may be transferrable to crop plants with an eye toward building a more sustainable agriculture. Science , this issue p. eaba6605

Fungal symbiosis with early land plants Hundreds of millions of years ago, evolved descendants of aquatic plants began showing up on dry land. These newly terrestrialized species had to deal with increased ultraviolet light exposure, desiccation, and less accessible nutrients. Rich et al. show how mutualist fungi may have helped these nascent plant lineages with adaptation to their newly challenging environment (see the Perspective by Bouwmeester). Genetic and metabolic analysis of a liverwort as a representative of such plants suggests that the mutually beneficial exchange of nutrients with arbuscular mycorrhizal fungi may have been a feature of these most early land plants. Science , abg0929, this issue p. 864 ; see also abi8016, p. 789

Fungi have crucial roles in modern ecosystems as decomposers and pathogens, and they engage in various mutualistic associations with other organisms, especially plants. They have a lengthy geological history, and there is an emerging understanding of their impact on the evolution of Earth systems on a large scale. In this Review, we focus on the roles of fungi in the establishment and early evolution of land and freshwater ecosystems. Today, questions of evolution over deep time are informed by discoveries of new fossils and evolutionary analysis of new genomes. Inferences can be drawn from evolutionary analysis by comparing the genes and genomes of fungi with the biochemistry and development of their plant and algal hosts. We then contrast this emerging picture against evidence from the fossil record to develop a new, integrated perspective on the origin and early evolution of fungi. Fungi originated in a freshwater environment and their evolution accompanied the rise of algae and land plants. In this Review, Berbee and colleagues examine the fossil and genomic record of ancient fungi and the inferences we can make about their lifestyle.

White lupin (Lupinus albus L.) is an annual crop cultivated for its protein-rich seeds. It is adapted to poor soils due to the production of cluster roots, which are made of dozens of determinate lateral roots that drastically improve soil exploration and nutrient acquisition (mostly phosphate). Using long-read sequencing technologies, we provide a high-quality genome sequence of a cultivated accession of white lupin (2n = 50, 451 Mb), as well as de novo assemblies of a landrace and a wild relative. We describe a modern accession displaying increased soil exploration capacity through early establishment of lateral and cluster roots. We also show how seed quality may have been impacted by domestication in term of protein profiles and alkaloid content. The availability of a high-quality genome assembly together with companion genomic and transcriptomic resources will enable the development of modern breeding strategies to increase and stabilize white lupin yield., White lupin is an annual crop cultivated for protein rich seeds and can produce cluster roots for efficient phosphate acquisition. Here, the authors generate high quality genome assemblies of a cultivated accession, a landrace, and a wild relative and provides insight into soil exploration and seed quality.

Plant cell infections are tightly orchestrated by cell wall (CW) alterations, plasma membrane (PM) resident signalling processes and dynamic remodelling of the cytoskeleton. During root nodule symbiosis these processes result in morpho-dynamic responses including root hair swelling and curling, PM invagination and polar growth of a tubular infection structure, the infection thread (IT). However, the molecular details driving and guiding these PM remodelling events remain to be unravelled. Here, we studied a formin protein (SYFO1) in M. truncatula that is specifically induced during rhizobial infection. Phenotypical analysis of syfo1 mutants clearly indicates that the encoded protein is required for efficient rhizobial colonization of root hairs. SYFO1 itself creates a proteinaceous bridge between the CW and the polarized cytoskeleton. It binds to CW components via a proline-rich N-terminal segment, which is indispensable for its function. On the cytoplasmic side of the PM SYFO1 is associated with actin accumulations supporting the hypothesis that it contributes to cell polarization in vivo. This is further sustained by the fact that cell shape changes can be induced in a stimulus-dependent manner in root protoplasts expressing SYFO1. Taken together we provide evidence for the evolutionary re-wiring of a generic cytoskeleton modulator into a symbiosis-specific response.

Nitrogen (N) is an essential macronutrient and a key cellular messenger. Plants have evolved refined molecular systems to sense the cellular nitrogen status. Exemplified by the root nodule symbiosis between legumes and symbiotic rhizobia, where external nitrate availability inhibits the interaction. However, nitrate also functions as a metabolic messenger, resulting in nitrate signaling cascades which intensively cross-talk with other physiological pathways. NIN (NODULE INCEPTION)-LIKE PROTEINS (NLPs) are key players in nitrate signaling and regulate nitrate-dependent transcription. Nevertheless, the coordinated interplay between nitrate signaling pathways and rhizobacteria-induced responses remains to be elucidated. In our study, we investigate rhizobia-induced changes in the root system architecture of the non-legume host Arabidopsis in dependence of different nitrate conditions. We demonstrate that rhizobia induce lateral root growth, and increase root hair length and density in a nitrate-dependent manner. These processes are regulated by AtNLP4 and AtNLP5 as well as nitrate transceptor NRT1.1, as the corresponding mutants fail to respond to rhizobia. On a cellular level,NLP4andNLP5control a rhizobia-induced decrease in cell elongation rates, while additional cell divisions occurred independent ofNLP4. In summary, our data suggest that root morphological responses to rhizobia, dependent on a nutritional signaling pathway that is evolutionary related to regulatory circuits described in legumes.

International audience; The quest for determining how looked like the plants that first lived on lands 450 million years ago is among the most exciting challenges in evolutionary biology. Recent works indicate that they displayed angiosperm-like stomata. Text: The ancestor of extant land plants diverged from the lineage leading to the Zygnematophyceae algae and gradually adapted to the terrestrial environment. Fossils of 450-475 million years old spore dyads and tetrads, which are structures associated only with land plant, are the first evidence of the changes in this branch of the green lineage [1]. Well-preserved fossil specimens tell us that less than 50 million years later the plant lineage had already diversified, with plants displaying subaerial and underground axes, and vasculature [2]. Between these two milestones: a gap of 50 million years devoid of known macrofossils, leaving a gap even wider in our understanding of plant evolution. The morphology, physiology and overall biology of the first land plants remain an absolute mystery. Although the hunt for fossils of the first land plants is ongoing, an alternative approach would be to infer, to predict, their morphology and physiology based on extant land plant species. For such an inference, an accurate understanding of the plant phylogeny and the precise description of the traits of interest across this phylogeny are needed [3]. In this issue of Current Biology Harris et al. (XXX) combined a consolidated plant phylogeny with the phylogenetic analysis of genes linked to stomata development to determine whether stomata were present in the most recent common ancestor (MRCA) of land plants. The monophyly of Bryophytes supported once again Resolving the deep nodes of the land-plant phylogeny, the ones close to their origin more than 450 million years ago, has been a major goal in evolutionary biology for decades. Over the last five years, the availability of newly sequenced genomes and transcriptomes combined with a wide array of molecular phylogenetic methods allowed two hypotheses to

International audience; Title: Evolution of plant metabolism: A (bio)synthesis Studying the evolution of metabolism is technically challenging. A novel study combining in silico metabolic maps and phylogenomics allows reconstructing the diversification of plant metabolism across one billion years of evolution. Text: Following the initial primary endosymbiotic event leading to the evolution of the chloroplast approximately a billion years ago, plants (Viridiplantae or Chloroplastida) have evolved into a tremendous diversity of organisms such as green algae, mosses or ferns [1]. Each of these lineages has evolved prominent developmental and physiological innovations linked to the colonization of new ecological niches. Although roots and flowers will come to everyone's mind when asked for plant innovations, one can hardly argue against specific metabolites, say caffeine, as iconic lineage-specific novelties. Besides such recent evolution, metabolic novelties that evolved at deep nodes in the plant phylogeny may have played essential roles in the evolution of extremely diverse and successful plant lineages such as the land plants. However, while scoring for the presence or absence of a given macroscopic trait-such as roots or flowers-is relatively straightforward, determining the distribution of metabolites requires the use of sophisticated and time-consuming approaches, hindering the description of the plant metabolism in an evolutionary perspective. In their work published in this issue of Current Biology Cannell et al. [2] overcome these limitations and propose a comprehensive view of the plant metabolism evolution. To do so, the authors first computed metabolic maps on eight focal taxa belonging to the major plant lineages. Rather than reflecting the presence or absence of a given enzymatic property, reconstructing biosynthesis pathways allow inferring whether the "modules" are present and thus the metabolic end-product. Mapping these predictions on the plant phylogeny, the authors were able to propose gains and losses of specific metabolic pathways in an untargeted manner. The initial set of eight species, although covering a large diversity of lineages, made the approach very sensitive to misannotation or assemblies. To strengthen their conclusions the authors included a total of 72 diverse plant genomes in an OrthoFinder run, identifying orthologs across all the species, and later added 305 transcriptomes. With these orthogroups, the authors were able to predict the evolution of the plant metabolism. Some of these predictions reflected the known evolutionary pattern of well-described metabolic pathways, such as the gain of thalianol biosynthesis in the Arabidopsis thaliana lineage [3] others turned out to be much more surprizing. Revisiting the evolution of plant hormones Gibberellins (GAs) are plant hormones regulating multiple developmental processes. Their biosynthesis is well described in angiosperms. Initial phylogenetic studies conducted on the biosynthetic enzymes on the model moss Physcomitrella patens, and metabolomics survey, suggested that active GAs (derivative of GA12) were not produced in mosses, suggesting that their evolution was specific to the vascular plants [4]. Here the authors discovered in liverworts and hornworts, the other two bryophyte clades, the entire suit of enzymes

International audience; The initiation of intracellular host cell colonization by symbiotic rhizobia in Medicago truncatula requires repolarization of root hairs, including the rearrangement of cytoskeletal filaments. The molecular players governing microtubule (MT) reorganization during rhizobial infections remain to be discovered. Here, we identified M. truncatula DEVELOPMENTALLY REGULATED PLASMA MEMBRANE POLYPEPTIDE (DREPP), a member of the MT binding DREPP/PCaP protein family, and investigated its functions during rhizobial infections. We show that rhizobial colonization of drepp mutant roots as well as transgenic roots overexpressing DREPP is impaired. DREPP relocalizes into symbiosis-specific membrane nanodomains in a stimulus-dependent manner. This subcellular segregation coincides with DREPP-dependent MT fragmentation and a partial loss of the ability to reorganize the MT cytoskeleton in response to rhizobia, which might rely on an interaction between DREPP and the MT-organizing protein SPIRAL2. Taken together, our results reveal that establishment of symbiotic associations in M. truncatula requires DREPP in order to regulate MT reorganization during initial root hair responses to rhizobia.

International audience; Plants are the foundation of terrestrial ecosystems, and their colonization of land was probably facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following this founding event, plant diversification has led to the emergence of a tremendous diversity of mutualistic symbioses with microorganisms, ranging from extracellular associations to the most intimate intracellular associations, where fungal or bacterial symbionts are hosted inside plant cells. Here, through analysis of 271 transcriptomes and 116 plant genomes spanning the entire land-plant diversity, we demonstrate that a common symbiosis signalling pathway co-evolved with intracellular endosymbioses, from the ancestral arbuscular mycorrhiza to the more recent ericoid and orchid mycorrhizae in angiosperms and ericoid-like associations of bryophytes. By contrast, species forming exclusively extracellular symbioses, such as ectomycorrhizae, and those forming associations with cyanobacteria, have lost this signalling pathway. This work unifies intracellular symbioses, revealing conservation in their evolution across 450 million yr of plant diversification.An extensive phylogenomics study based on hundreds of genomes and transcriptomes provides a new interpretation of the evolution of different types of symbiotic associations in land plants, and reveals a conserved ancestral symbiosis pathway.

Hornworts comprise a bryophyte lineage that diverged from other extant land plants >400 million years ago and bears unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis and a pyrenoid-based carbon-concentrating mechanism (CCM). Here, we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses place hornworts as a sister clade to liverworts plus mosses with high support. The Anthoceros genomes lack repeat-dense centromeres as well as whole-genome duplication, and contain a limited transcription factor repertoire. Several genes involved in angiosperm meristem and stomatal function are conserved in Anthoceros and upregulated during sporophyte development, suggesting possible homologies at the genetic level. We identified candidate genes involved in cyanobacterial symbiosis and found that LCIB, a Chlamydomonas CCM gene, is present in hornworts but absent in other plant lineages, implying a possible conserved role in CCM function. We anticipate that these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants., Analyses of three high-quality genomes of Anthoceros hornworts place hornworts as a sister clade to the lineage including liverworts and mosses, and provide insights into the unique biological features of hornworts.

The VAPYRIN (VPY) gene in Medicago truncatula and Petunia hybrida is required for arbuscular mycorrhizal (AM) symbiosis. The moss Physcomitrella patens has a close homologue (VPY-like, VPYL), although it does not form AM. Here, we explore the phylogeny of VPY and VPYL in land plants, and we study the expression and developmental function of VPYL in P. patens. We show that PpVPYL is expressed primarily in the protonema, the early filamentous stage of moss development, and later in rhizoids arising from the leafy gametophores and in adult phyllids. Knockout mutants have specific phenotypes in branching of the protonema and in cell division of the leaves (phyllids) in gametophores. The mutants are responsive to auxin and strigolactone, which are involved in the regulation of protonemal branching, indicating that the mutants are not affected in hormonal signaling. Taken together, these results suggest that PpVPYL exerts negative regulation of protonemal branching and of cell division in phyllids. We discuss VPY and VPYL phylogeny and function in land plants in the context of AM symbiosis in angiosperms, and of development in the moss.

The transition to a terrestrial environment, termed terrestrialization, is generally regarded as a pivotal event in the evolution and diversification of the land plant flora that changed the surface of our planet. Through phylogenomic studies, a group of streptophyte algae, the Zygnematophyceae, have recently been recognized as the likely sister group to land plants (embryophytes). Here, we report genome sequences and analyses of two early diverging Zygnematophyceae (Spirogloea muscicola gen. nov. and Mesotaenium endlicherianum) that share the same subaerial/terrestrial habitat with the earliest-diverging embryophytes, the bryophytes. We provide evidence that genes (i.e., GRAS and PYR/PYL/RCAR) that increase resistance to biotic and abiotic stresses in land plants, in particular desiccation, originated or expanded in the common ancestor of Zygnematophyceae and embryophytes, and were gained by horizontal gene transfer (HGT) from soil bacteria. These two Zygnematophyceae genomes represent a cornerstone for future studies to understand the underlying molecular mechanism and process of plant terrestrialization.

Plants are the foundation of terrestrial ecosystems and their colonization of land was facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following that founding event, plant diversification has led to the emergence of a tremendous diversity of mutualistic symbioses with microorganisms, ranging from extracellular associations to the most intimate intracellular associations, where fungal or bacterial symbionts are hosted inside plant cells. Through analysis of 271 transcriptomes and 122 plant genomes, we demonstrate that the common symbiosis signalling pathway controlling the association with arbuscular mycorrhizal fungi and with nitrogen-fixing bacteria specifically co-evolved with intracellular endosymbioses, including ericoid and orchid mycorrhizae in angiosperms and ericoid-like associations of bryophytes. In contrast, species forming exclusively extracellular symbioses like ectomycorrhizae or associations with cyanobacteria have lost this signalling pathway. This work unifies intracellular symbioses, revealing conservation in their evolution across 450 million years of plant diversification.

The initiation of intracellular host cell colonization by symbiotic rhizobia in Medicago truncatula requires repolarization of root hairs, which includes the re-arrangement of cytoskeletal filaments. The molecular players governing microtubule (MT) re-organization during infection remain to be discovered. Here, we identified the M. truncatula DREPP protein and investigated its functions during rhizobial infections. We show that rhizobial colonization of drepp mutant roots as well as transgenic roots over-expressing DREPP is impaired. DREPP re-localizes into symbiosis-specific membrane nanodomains in a stimulus-dependent manner. This subcellular segregation coincides with DREPP-dependent MT fragmentation and a partial loss of the ability to re-organize the MT cytoskeleton in response to rhizobia, which might relay on an interaction between DREPP and MT organizing protein SPIRAL2 (SPR2). Taken together, our results reveal that establishment of symbiotic associations in M. truncatula require DREPP in order to regulate MT reorganization during initial root hair responses to rhizobia.

The

International audience; Our planet is teeming with an astounding diversity of plants. In a mere single group of closely related species, tremendous diversity can be observed in their form and function - the colour of petals in flowering plants, the shape of the fronds in ferns, and the branching pattern of the gametophyte in mosses. Diversity can also be found in subtler traits, such as the resistance to pathogens or the ability to recruit symbiotic microbes from the environment. Plant traits can also be highly conserved - at the cellular and metabolic levels, entire biosynthetic pathways are present in all plant groups, and morphological characteristics such as vascular tissues have been conserved for hundreds of millions of years. The research community that seeks to understand these traits - both the diverse and the conserved - by taking an evolutionary point-of-view on plant biology is growing. Here, we summarize a subset of the different aspects of plant evolutionary biology, provide a guide for structuring comparative biology approaches and discuss the pitfalls that (plant) researchers should avoid when embarking on such studies.

White lupin (Lupinus albus L.) is a legume that produces seeds recognized for their high protein content and good nutritional value (lowest glycemic index of all grains, high dietary fiber content, and zero gluten or starch)1–5. White lupin can form nitrogen-fixing nodules but has lost the ability to form mycorrhizal symbiosis with fungi6. Nevertheless, its root system is well adapted to poor soils: it produces cluster roots, constituted of dozens of determinate lateral roots that improve soil exploration and phosphate remobilization7. As phosphate is a limited resource that comes from rock reserves8, the production of cluster roots is a trait of interest to improve fertilizers efficiency. Using long reads sequencing technologies, we provide a high-quality genome sequence of a modern variety of white lupin (2n=50, 451 Mb), as well asde novoassemblies of a landrace and a wild relative. We describe how domestication impacted soil exploration capacity through the early establishment of lateral and cluster roots. We identify theAPETALA2transcription factorLaPUCHI-1, homolog of the Arabidopsis morphogenesis coordinator9, as a potential regulator of this trait. Our high-quality genome and companion genomic and transcriptomic resources enable the development of modern breeding strategies to increase and stabilize yield and to develop new varieties with reduced allergenic properties (caused by conglutins10), which would favor the deployment of this promising culture.

'Summary' 89 I. 'Introduction' 89 II. 'AM symbiosis in plants: one gain and multiple losses' 90 III. 'Evolution of AM symbiosis-related genes' 90 IV. 'Discovery of new symbiotic genes' 91 V. 'Future perspectives' 92 VI. 'Conclusion' 93 References 93 Summary Understanding the genetic bases of complex traits has been a main challenge in biology for decades. Comparative phylogenomics offers an opportunity to identify candidate genes associated with these complex traits. This approach initially developed in prokaryotes consists in looking at shared coevolution between genes and traits. It thus requires a precise reconstruction of the trait evolution, a large genomic sampling in the clades of interest and an accurate definition of orthogroups. Recently, with the growing body of sequenced plant genomes, comparative genomics has been successfully applied to plants to study the widespread arbuscular mycorrhizal symbiosis. Here I will use these findings to illustrate the main principles of comparative phylogenomic approaches and propose directions to improve our understanding of symbiotic associations.

Signals and signaling pathways underlying the symbiosis between legumes and rhizobia have been studied extensively over the past decades. In a previous phosphoproteomic study on the Medicago truncatula–Sinorhizobium meliloti symbiosis, we identified plant proteins that are differentially phosphorylated upon the perception of rhizobial signals, called Nod factors. In this study, we provide experimental evidence that one of these proteins, Early Phosphorylated Protein 1 (EPP1), is required for the initiation of this symbiosis. Upon inoculation with rhizobia, MtEPP1 expression was induced in curled root hairs. Down-regulation of MtEPP1 in M. truncatula roots almost abolished calcium spiking, reduced the expression of essential symbiosis-related genes (MtNIN, MtNF-YB1, MtERN1 and MtENOD40) and strongly decreased nodule development. Phylogenetic analyses revealed that orthologs of MtEPP1 are present in legumes and specifically in plant species able to host arbuscular mycorrhizal fungi, suggesting a possible role in this association too. Short chitin oligomers induced the phosphorylation of MtEPP1 like Nod factors. However, the down-regulation of MtEPP1 affected the colonization of M. truncatula roots by arbuscular mycorrhizal fungi only moderately. Altogether, these findings indicate that MtEPP1 is essential for the establishment of the legume–rhizobia symbiosis but might plays a limited role in the arbuscular mycorrhizal symbiosis.

Understanding plant evolution and diversity in a phylogenomic context is an enormous challenge due, in part, to limited availability of genome-scale data across phylodiverse species. The 10KP (10,000 Plants) Genome Sequencing Project will sequence and characterize representative genomes from every major clade of embryophytes, green algae, and protists (excluding fungi) within the next 5 years. By implementing and continuously improving leading-edge sequencing technologies and bioinformatics tools, 10KP will catalogue the genome content of plant and protist diversity and make these data freely available as an enduring foundation for future scientific discoveries and applications. 10KP is structured as an international consortium, open to the global community, including botanical gardens, plant research institutes, universities, and private industry. Our immediate goal is to establish a policy framework for this endeavor, the principles of which are outlined here.

The root nodule symbiosis of plants with nitrogen-fixing bacteria affects global nitrogen cycles and food production but is restricted to a subset of genera within a single clade of flowering plants. To explore the genetic basis for this scattered occurrence, we sequenced the genomes of 10 plant species covering the diversity of nodule morphotypes, bacterial symbionts, and infection strategies. In a genome-wide comparative analysis of a total of 37 plant species, we discovered signatures of multiple independent loss-of-function events in the indispensable symbiotic regulator NODULE INCEPTION in 10 of 13 genomes of nonnodulating species within this clade. The discovery that multiple independent losses shaped the present-day distribution of nitrogen-fixing root nodule symbiosis in plants reveals a phylogenetically wider distribution in evolutionary history and a so-far-underestimated selection pressure against this symbiosis. Fil: Griesmann, Maximilian. Ludwig Maximilians Universitat; Alemania Fil: Chang, Yue. No especifíca; Fil: Liu, Xin. No especifíca; Fil: Song, Yue. No especifíca; Fil: Haberer, Georg. Helmholtz Center Munich; Alemania Fil: Crook, Matthew B.. Weber State University; Estados Unidos Fil: Billault-Penneteau, Benjamin. Ludwig Maximilians Universitat; Alemania Fil: Lauressergues, Dominique. Université de Toulouse; Francia Fil: Keller, Jean. Université de Toulouse; Francia Fil: Imanishi, Leandro Ezequiel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Roswanjaya, Yuda Purwana. University of Agriculture Wageningen; Países Bajos Fil: Kohlen, Wouter. University of Agriculture Wageningen; Países Bajos Fil: Pujic, Petar. Université de Lyon; Francia Fil: Battenberg, Kai. University of California at Davis; Estados Unidos Fil: Alloisio, Nicole. No especifíca; Fil: Liang, Yuhu. No especifíca; Fil: Hilhorst, Henk. No especifíca; Fil: Salgado, Marco G.. Stockholms Universitet; Suecia Fil: Hocher, Valerie. Université Montpellier II; Francia Fil: Gherbi, Hassen. Université Montpellier II; Francia Fil: Svistoonoff, Sergio. Université Montpellier II; Francia Fil: Doyle, Jeff J.. Cornell University; Estados Unidos Fil: He, Shixu. No especifíca; Fil: Xu, Yan. China National Genebank; China Fil: Xu, Shanyun. China National Genebank; China Fil: Qu, Jing. China National Genebank; China Fil: Gao, Qiang. No especifíca; Fil: Fang, Xiaodong. No especifíca; Fil: Fu, Yuan. China National Genebank; China Fil: Normand, Philippe. Universite Lyon 2; Francia Fil: Berry, Alison M.. University of California at Davis; Estados Unidos Fil: Wall, Luis Gabriel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Ané, Jean Michel. University of Wisconsin; Estados Unidos Fil: Pawlowski, Katharina. Stockholms Universitet; Suecia Fil: Xu, Xun. China National Genebank; China Fil: Yang, Huanming. James D. Watson Institute Of Genome Sciences; China Fil: Spannagl, Manuel. Helmholtz Center Munich German Research Center For Environmental Health; Alemania Fil: Mayer, Klaus F.X.. Helmholtz Center Munich German Research Center For Environmental Health; Alemania Fil: Wong, Gane Ka-Shu. University of Alberta; Canadá Fil: Parniske, Martin. Ludwig Maximilians Universitat; Alemania Fil: Delaux, Pierre Marc. No especifíca; Fil: Cheng, Shifeng. China National Genebank; China

The draft genome of Chara braunii reveals many plant-like features important for colonization of land that evolved in charophytic algae and therefore prior to the earliest land plants. Land plants evolved from charophytic algae, among which Charophyceae possess the most complex body plans. We present the genome of Chara braunii; comparison of the genome to those of land plants identified evolutionary novelties for plant terrestrialization and land plant heritage genes. C. braunii employs unique xylan synthases for cell wall biosynthesis, a phragmoplast (cell separation) mechanism similar to that of land plants, and many phytohormones. C. braunii plastids are controlled via land-plant-like retrograde signaling, and transcriptional regulation is more elaborate than in other algae. The morphological complexity of this organism may result from expanded gene families, with three cases of particular note: genes effecting tolerance to reactive oxygen species (ROS), LysM receptor-like kinases, and transcription factors (TFs). Transcriptomic analysis of sexual reproductive structures reveals intricate control by TFs, activity of the ROS gene network, and the ancestral use of plant-like storage and stress protection proteins in the zygote. © 2018 Elsevier Inc.

Colonization of land by plants was a major transition on Earth, but the developmental and genetic innovations required for this transition remain unknown. Physiological studies and the fossil record strongly suggest that the ability of the first land plants to form symbiotic associations with beneficial fungi was one of these critical innovations. In angiosperms, genes required for the perception and transduction of diffusible fungal signals for root colonization and for nutrient exchange have been characterized. However, the origin of these genes and their potential correlation with land colonization remain elusive. A comprehensive phylogenetic analysis of 259 transcriptomes and 10 green algal and basal land plant genomes, coupled with the characterization of the evolutionary path leading to the appearance of a key regulator, a calcium- and calmodulin-dependent protein kinase, showed that the symbiotic signaling pathway predated the first land plants. In contrast, downstream genes required for root colonization and their specific expression pattern probably appeared subsequent to the colonization of land. We conclude that the most recent common ancestor of extant land plants and green algae was preadapted for symbiotic associations. Subsequent improvement of this precursor stage in early land plants through rounds of gene duplication led to the acquisition of additional pathways and the ability to form a fully functional arbuscular mycorrhizal symbiosis.

Nitrogen-fixing symbioses between plants and bacteria are restricted to a few plant lineages. The plant partner benefits from these associations by gaining access to the pool of atmospheric nitrogen. By contrast, other plant species, including all cereals, rely only on the scarce nitrogen present in the soil and what they can glean from associative bacteria. Global cereal yields from conventional agriculture are dependent on the application of massive levels of chemical fertilisers. Engineering nitrogen-fixing symbioses into cereal crops could in part mitigate the economic and ecological impacts caused by the overuse of fertilisers and provide better global parity in crop yields. Comparative phylogenetics and phylogenomics are powerful tools to identify genetic and genomic innovations behind key plant traits. In this review we highlight recent discoveries made using such approaches and we discuss how these approaches could be used to help direct the engineering of nitrogen-fixing symbioses into cereals.

Premise of research. The origin of land plants catalyzed key changes in Earth’s atmosphere and biota. Microbial associations likely nurtured earliest plants and influenced their biogeochemical roles. Because angiosperm and animal microbiomes—bacteria, archaea, microbial eukaryotes, and genes that promote host survival—are known to display lineage effects, we hypothesized that microbiomes of early-diverging modern bryophytes and phylogenetically closely related green algae might likewise reveal commonalities reflecting ancestral traits.Methodology. New metagenomic sequence data were obtained for the late-diverging streptophyte algae Chaetosphaeridium globosum and Coleochaete pulvinata and the liverwort Conocephalum conicum, representing early-diverging land plants. New 16S rDNA amplicon sequences were acquired for the charalean Nitella tenuissima. Sequence data were used to infer bacterial genera and fungi for comparisons among streptophyte microbiota and with our published microbiome data for the outgroup...